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Xiaotong Wu X Wu, college of animal sciences, Zhejiang University, Hangzhou, China

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Yan Shi Y Shi, college of animal sciences, Zhejiang University, Hangzhou, China

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Bingjie Hu B Hu, college of animal sciences, Zhejiang University, Hangzhou, China

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Panpan Zhao P Zhao, college of animal sciences, Zhejiang University, Hangzhou, China

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Shuang Li S Li, college of animal sciences, Zhejiang University, Hangzhou, China

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Lieying Xiao L Xiao, college of animal sciences, Zhejiang University, Hangzhou, China

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Shaohua Wang S Wang, college of animal sciences, Zhejiang University, Hangzhou, China

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Kun Zhang K Zhang, college of animal sciences, Zhejiang University, Hangzhou, China

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Tead4, a critical transcription factor expressed during preimplantation development, is essential for the expression of trophectoderm-specific genes in mice. However, the functional mechanism of TEAD4 in mouse preimplantation development and its conservation across mammals remain unclear. Here, we report that Tead4 is a crucial transcription factor necessary for blastocyst formation in mice. Disruption of Tead4 through base editing results in developmental arrest at the morula stage. Additionally, RNA-seq analysis reveals dysregulation of 670 genes in Tead4 knockout embryos. As anticipated, Tead4 knockout led to a decrease in trophectoderm genes Cdx2 and Gata3. Intriguingly, we observed a reduction in Krt8, suggesting that Tead4 influences the integrity of the trophectoderm epithelium in mice. More importantly, we noted a dramatic decrease in nuclear Yap in outside cells for Tead4-deficient morula, indicating that Tead4 directly regulates Hippo signaling. In contrast, bovine embryos with TEAD4 depletion could still develop to blastocysts with normal expression of CDX2, GATA3, and SOX2, albeit with a decrease in total cell number and ICM cell number. In conclusion, we propose that Tead4 regulates mouse blastocyst formation via Krt8 and Yap, both of which are critical regulators of mouse preimplantation development.

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Yan Shi Laboratory of Mammalian Molecular Embryology, College of Animal Sciences, Zhejiang University, Hangzhou, China

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Bingjie Hu Laboratory of Mammalian Molecular Embryology, College of Animal Sciences, Zhejiang University, Hangzhou, China

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Zizengchen Wang Laboratory of Mammalian Molecular Embryology, College of Animal Sciences, Zhejiang University, Hangzhou, China

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Xiaotong Wu Laboratory of Mammalian Molecular Embryology, College of Animal Sciences, Zhejiang University, Hangzhou, China

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Lei Luo Laboratory of Mammalian Molecular Embryology, College of Animal Sciences, Zhejiang University, Hangzhou, China

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Shuang Li Laboratory of Mammalian Molecular Embryology, College of Animal Sciences, Zhejiang University, Hangzhou, China

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Shaohua Wang Laboratory of Mammalian Molecular Embryology, College of Animal Sciences, Zhejiang University, Hangzhou, China

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Kun Zhang Laboratory of Mammalian Molecular Embryology, College of Animal Sciences, Zhejiang University, Hangzhou, China

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Huanan Wang Laboratory of Mammalian Molecular Embryology, College of Animal Sciences, Zhejiang University, Hangzhou, China

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In brief

The lineage specification during early embryonic development in cattle remains largely elusive. The present study determines the effects of trophectoderm-associated factors GATA3 and CDX2 on lineage specification during bovine early embryonic development.

Abstract

Current understandings of the initiation of the trophectoderm (TE) program during mammalian embryonic development lack evidence of how TE-associated factors such as GATA3 and CDX2 participate in bovine lineage specification. In this study, we describe the effects of TE-associated factors on the expression of lineage specification marker genes such as SOX2, OCT4, NANOG, GATA6, and SOX17, by using cytosine base editor system. We successfully knockout GATA3 or CDX2 in bovine embryos with a robust efficiency. However, GATA3 or CDX2 deletion does not affect the developmental potential of embryos to reach the blastocyst stage. Interestingly, GATA3 deletion downregulates the NANOG expression in bovine blastocysts. Further analysis of the mosaic embryos shows that GATA3 is required for NANOG in the TE of bovine blastocysts. Single blastocyst RNA-seq analysis reveals that GATA3 deletion disrupts the transcriptome in bovine blastocysts. Altogether, we propose that GATA3 plays an important role in maintaining TE lineage program in bovine embryos and the functional role of GATA3 is species-specific.

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Xiaotong Wu Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang, China

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Yan Shi Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang, China

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Bingjie Hu Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang, China

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Panpan Zhao Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang, China

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Shuang Li Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang, China

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Lieying Xiao Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang, China

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Shaohua Wang Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang, China

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Kun Zhang Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou, Zhejiang, China

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In brief

Lineage specification plays a vital role in preimplantation development. TEAD4 is an essential transcription factor for trophectoderm lineage specification in mice but not in cattle.

Abstract

Tead4, a critical transcription factor expressed during preimplantation development, is essential for the expression of trophectoderm-specific genes in mice. However, the functional mechanism of TEAD4 in mouse preimplantation development and its conservation across mammals remain unclear. Here, we report that Tead4 is a crucial transcription factor necessary for blastocyst formation in mice. Disruption of Tead4 through base editing results in developmental arrest at the morula stage. Additionally, RNA-seq analysis reveals dysregulation of 670 genes in Tead4 knockout embryos. As anticipated, Tead4 knockout led to a decrease in trophectoderm genes Cdx2 and Gata3. Intriguingly, we observed a reduction in Krt8, suggesting that Tead4 influences the integrity of the trophectoderm epithelium in mice. More importantly, we noted a dramatic decrease in nuclear Yap in outside cells for Tead4-deficient morula, indicating that Tead4 directly regulates Hippo signaling. In contrast, bovine embryos with TEAD4 depletion could still develop to blastocysts with normal expression of CDX2, GATA3, and SOX2, albeit with a decrease in total cell number and ICM cell number. In conclusion, we propose that Tead4 regulates mouse blastocyst formation via Krt8 and Yap, both of which are critical regulators of mouse preimplantation development.

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